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Gene of Klebsiella Oxytoca

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Gene of Klebsiella Oxytoca Biosci. Biotechnol. Biochem., 72 (1), 116–123, 2008 Identification of the 4-Hydroxycinnamate Decarboxylase (PAD) Gene of Klebsiella oxytoca y Hirofumi UCHIYAMA, Yasuyuki HASHIDOKO, Yuhki KURIYAMA, and Satoshi TAHARA Division of Applied Bioscience, Research Faculty of Agriculture, Hokkaido University, Kita-ku, Sapporo 060-8589, Japan Received August 3, 2007; Accepted October 15, 2007; Online Publication, January 7, 2008 [doi:10.1271/bbb.70496] A 7.1-kbp DNA fragment isolated from a wild strain also a synonym of phenylacrylic acid decarboxylase, of Klebsiella oxytoca was sequenced, leading to the PAD) to utilize the decarboxylative product, 4-hydroxy- identification of 10 open-reading frames (ORFs), in- lated styrene, as an antifungal agent.3) In 1994, Hashi- cluding a 504-bp Pad gene. The Pad gene of the Gram- doko et al. successfully cloned the Pad gene from a negative bacterium was subsequently expressed in genomic library prepared from wild-type K. oxytoca.4) A Escherichia coli as a chimeric Pad. The deduced amino 9.6-kbp genomic fragment carrying the Pad gene was acid (AA) sequence of the Pad gene from wild-type obtained using Cladosporium herbarum AHU 9262 as a K. oxytoca showed approximately 50% homology to bioindicator which was highly sensitive to 4-hydroxy- those of other bacterial PADs from Gram-positive styrene produced from 4-hydroxycinnamic acid via PAD bacilli plus a coccus. These data and a genomic library catalytic decarboxylation. Transformed Escherichia search of some -proteobacteria, including E. coli and coli JM 109 harboring the cloned Pad gene region Vibrio sp., indicated that PAD of K. oxytoca is a member acquired the ability to decarboxylate (E)-4-hydroxycin- of the bacterial PAD family characteristic of Gram- namate into 4-hydroxystyrene. Digestion with SacI and negative bacteria. Using Pad-specific PCR primers EcoRI cleaved this 9.6-kbp DNA region into three designed from the Gram-negative bacterial Pad of fragments: HindIII-EcoRI (2.4 kbp, fragment C), EcoRI- K. oxytoca, Pad genes of two further strains of K. oxy- SacI (4.7 kbp, fragment B), and SacI-HindIII (2.5 kbp, toca, another wild isolate and JCM 1665 and two PAD- fragment A). These three fragments were independently positive Enterobacter spp. were successfully amplified cloned into the pUC19 vector. The expression of Pad in for specific Pad detection. each fragment in transformed E. coli was unsuccessful. Only bacterial cells transformed with recombinant DNA Key words: Klebsiella oxytoca; bacterial Pad gene; PCR containing fragment CB (7.1 kbp, HindIII-SacI possess- detection of Pad; Gram-negative bacteria; ing an EcoRI site inside the DNA sequence) gained the 4-hydroxycinnamate decarboxylase gene ability to decarboxylate 4-hydroxycinnamic acid (un- published data), but the DNA sequence of the Pad gene Some plant families, such as Convolvulaceae, Aster- on fragment CB has not yet been characterized. iaceae, and Umbelliferae, are representative chlorogenic Bacterial Pad gene studies have been done in food acid-accumulating plant families that contain high chemistry, due to serious issues of off-flavor during the concentrations of hydroxycinnamoyl quinic acids in fermentation of foods and liquor. In 1995, bacterial Pad their leaves and/or roots. Many of these plant poly- of Gram-positive Bacillus pumilis was first characterized phenols are now recognized as self-defensive substan- by Zago et al., and a full-length amino acid (AA) ces, but the roles of these plant products in interactions sequence of PAD was deduced.5) Since this identifica- between polyphenol-rich plants and host-associating tion of Pad, additional Pad genes have been charac- microorganisms are not well understood.1,2) In 1993, terized in more than 20 different microorganisms, but Hashidoko et al. investigated phylloplane bacteria from almost all of these microorganisms are Gram-positive the chlorogenic acid-accumulating plant Polymnia son- bacilli plus a coccus.6–8) In contrast, among Gram- chifolia, a member of the Asteriaceae family. A phyllo- negative bacteria, only Pseudomonas fluorescens9) and plane bacterium was tentatively identified as Klebsiella K. oxytoca10) have been reported to possess PAD oxytoca by morphological and biochemical character- activity in crude protein from bacterial cells. Bacterial ization. This organism was found actively to decarbox- Pad-like ORFs have been found in genomic DNA from ylate 4-hydroxylated cinnamic acids by a substrate- two Gram-negative proteobacteria, Vibrio cholerae and inducible 4-hydroxycinnamate decarboxylase (4-HCD; Erwinia carotovora,11,12) but it is uncertain whether the y To whom correspondence should be addressed. Fax: +81-11-706-4182; E-mail: [email protected] Identification of Pad Gene from Klebsiella oxytoca 117 encoded gene products possess PAD functionality in Characterization of ORF regions in fragment CB. The vivo. Hence both the enzymatic and the bacterio- target DNA (fragment CB), possessing 7,102 bp between physiological traits of PAD have yet to be examined the HindIII and SacI sites, did not contain any regions in Gram-negative bacteria. In fact, the physiological and that exhibited high homology to Pad of Bacillus spp. ecological roles of PAD-producing bacteria and PAD Hence all of the ORF regions on this DNA fragment itself in the terrestrial ecosystem are unclear, because were searched by means of an ORF Finder tool provided K. oxytoca immediately hydrolyzed chlorogenic acid to by NCBI (http://www.ddbj.nig.ac.jp/search/blast-j.html). yield 4-hydroxylated styrenes in chlorogenic acid-con- ORF regions were searched from both plus and minus taining potato-dextrose medium.13) In this study, we strand directions with putative amino acid translations aimed to determine the DNA sequence of Pad in from three different frames (+1, +2, +3, À1, À2, and fragment CB originating in epiphytic K. oxytoca, and to À3). A total of 20 ORF candidates of 250 bp or greater describe the PADs of other strains of K. oxytoca and two were identified on the target DNA. The deduced amino further wild isolates of Enterobacter spp. acid (AA) sequences of the putative proteins encoded on each ORF were further searched on the BLASTX Materials and Methods database of DDBJ (http://www.ddbj.nig.ac.jp/search/ blast-j.html). General. The 7.1-kb DNA fragment (fragment CB) carrying the gene for PAD was identical to one Design of adapter primers for Pad gene insertion into previously cloned from chromosomal DNA of a wild- pGEX 4T-3. In order to sub-clone target ORF regions into type K. oxytoca bacterial strain. This DNA fragment the pGEX vector, adapter primers were designed on the possessed HindIII and SacI sites at the 50 and 30 ends SIGMA Genosys website (http://www.genosys.jp/adt/ respectively, and it was cloned into pUC19 vector SGJ NN 3rd.html), and predictions for Tm, hairpin, and plasmid. For PCR, HotStarTaq (Qiagen, Germantown, dimer structures were obtained. The designed adapter MD) was used at 97 C for 15 min for preliminary primers were: PAD-APF (forward, 50-CGGAATTC- heating. The reaction conditions are described in detail TATGAGCACATTCGACAAACA-30, 29 mer, Tm ¼ for each experiment below. DNA and amino acid (AA) 73 C), and PAD-APR (reverse, 50-CGCTCGAGGAT- sequence homology searches were performed on the TACAGGTTGGCAGGAA-30, 27 mer, Tm ¼ 77 C). website of NCBI (National Center for Biotechnology These primers possessed EcoRI and XhoI restriction Information, USA) and DDBJ (DNA Data Bank of sites at the 50 and 30 ends respectively. The specificity of Japan, Mishima, Japan). the primers was confirmed by PCR using fragment CB as the source of template DNA. PCR conditions were as Primer design for direct sequencing. The primers follows for the amplification of the ORF-7 regions: 30 used in this study are shown in Table 1. Based upon the cycles of denaturation at 94 C for 1 min, annealing at sequence determination obtained from the initial round 50 C for 1 min, and extension at 72 C for 1 min. of sequencing, we designed customized forward/reverse The resulting PCR product (523 bp) was double- internal primers. The DNA sequence of fragment CB digested with EcoRI and XhoI, and the enzymes were was registered in the DDBJ DNA data bank under denatured by heating. The digested PCR product was accession no. AB330293. then ligated into pGEX 4T-3 expression vector (Amer- sham Pharmacia Biotech, Uppsala, Sweden) at the EcoRI-XhoI cloning site for in-frame fusion to the Table 1. Primers Used in Sequencing of Fragment CB internal GST gene in pGEX 4T-3. A set of adapter primers (À1, AP3, and AP4) was designed for Pad 50-GTTCCACGGTCTCTTCC-30 (160–176) 50-GATGTTGATGATCTGCC-30 (395–411) expression. The ligation reaction was set at a molar ratio 50-GGATAATCTTCAGGTTCTC-30 (837–856) of the vector plasmid:PCR product = 1:10. E. coli cells 50-GTTTCGCTTTCACCGT-30 (1,707–1,722) were transformed with the recombinant plasmid to 50-ATGTCATCGCACAGCA-30 (1,815–1,830) 0 0 facilitate the production of recombinant, PAD GST- 5 -CATCCCGACGAACTGG-3 (2,208–2,221) fusion protein. Transformed cells were assayed for PAD 50-AGAGCGATGACGCTGCCGAA-30 (2,336–2,355) 50-GGATCTCAACCG-30 (2,474–2,486) activity with a decarboxylation test in the cultured 10) 50-GTTGATCATCTTCGAGG-30 (2,635–2,651) medium using (E)-caffeic acid as the substrate. 50-GCTTCGGTGAGCAT-30 (2,888–2,901) 50-GAGTCATCGCTGCT-30 (2,909–2,922) Confirmation of PAD activity in transformed 0 0 E. coli 5 -AGCTCGCGCAGATAG-3 (3,399–3,413) with recombinant pGEX 4T-3 plasmid. E. coli JM109 50-GGATAATTGCTTTGGTTC-30 (3,832–3,849) 50-CGTGAAACAGTTTATCG-30 (4,843–4,859) competent cells (Nippon Gene, Toyama, Japan) were 50-GTCGGTGAGCTATAATCTC-30 (5,412–5,430) transformed with the recombinant pGEX 4T-3PAD 50-ATGCGGTGCTGTATCAG-30 (5,974–5,990) plasmid carrying the Pad gene.
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